Nucleolar stress regulates stromal–epithelial transition via NPM1 during decidualization

in Reproduction
View More View Less
  • 1 Shanxi Key Laboratory of Birth Defect and Cell Regeneration, Shanxi Medical University, Taiyuan, China
  • 2 College of Veterinary Medicine, South China Agricultural University
  • 3 College of Life Science and Resources and Environment, Yichun University, Yichun, China
  • 4 Reproductive Medicine Center, Renmin Hospital, Hubei University of Medicine, Shiyan, Hubei, China

Correspondence should be addressed and reprint requests to Z-M Yang; Email: zmyang@scau.edu.cn
Restricted access

Embryo implantation and decidualization are crucial steps during early pregnancy. We recently showed that nucleolar stress is involved in embryo implantation. This study was to explore whether nucleolar stress participates in mouse and human decidualization. Our data demonstrated that a low dose of actinomycin D (ActD) could induce nucleolar stress in stroma cells. Nucleolar stress promotes the stromal-epithelial transition during mouse in vitro decidualization through nucleophosmin1 (NPM1). Under nucleolar stress, Wnt family member 4 (Wnt4), a decidualization marker, is significantly increased, but decidua/trophoblast prolactin-related protein (Dtprp/Prl8a2) expression remains unchanged. For translational significance, we also examined the effects of nucleolar stress on human decidualization. Nucleolar stress stimulated by a low dose of ActD enhances human stromal–epithelial transition during human decidualization, but has no effects on the expression of insulin-like growth factor-binding protein 1 (IGFBP1). Our study indicates that nucleolar stress may promote only the mesenchymal–epithelial transition (MET), but not for all the molecular changes during decidualization.

 

     An official journal of

    Society for Reproduction and Fertility

 

Sept 2018 onwards Past Year Past 30 Days
Abstract Views 249 249 164
Full Text Views 20 20 14
PDF Downloads 17 17 13
  • Agarwal A, Gupta S & Sharma RK 2005 Role of oxidative stress in female reproduction. Reproductive Biology and Endocrinology 3 28. (https://doi.org/10.1186/1477-7827-3-28)

    • Search Google Scholar
    • Export Citation
  • Al-Sabbagh M, Fusi L, Higham J, Lee Y, Lei K, Hanyaloglu AC, Lam EW, Christian M & Brosens JJ 2011 NADPH oxidase-derived reactive oxygen species mediate decidualization of human endometrial stromal cells in response to cyclic AMP signaling. Endocrinology 152 730740. (https://doi.org/10.1210/en.2010-0899)

    • Search Google Scholar
    • Export Citation
  • Avitabile D, Bailey B, Cottage CT, Sundararaman B, Joyo A, Mcgregor M, Gude N, Truffa S, Zarrabi A & Konstandin M 2011 Nucleolar stress is an early response to myocardial damage involving nucleolar proteins nucleostemin and nucleophosmin. PNAS 108 61456150. (https://doi.org/10.1073/pnas.1017935108)

    • Search Google Scholar
    • Export Citation
  • Bhat KP, Itahana K, Jin A & Zhang Y 2004 Essential role of ribosomal protein L11 in mediating growth inhibition-induced p53 activation. The EMBO Journal 23 24022412. (https://doi.org/10.1038/sj.emboj.7600247)

    • Search Google Scholar
    • Export Citation
  • Bonner WM, Redon CE, Dickey JS, Nakamura AJ, Sedelnikova OA, Solier S & Pommier Y 2008 GammaH2AX and cancer. Nature Reviews: Cancer 8 957967. (https://doi.org/10.1038/nrc2523)

    • Search Google Scholar
    • Export Citation
  • Boulon S, Westman BJ, Hutten S, Boisvert FM & Lamond AI 2010 The nucleolus under stress. Molecular Cell 40 216227. (https://doi.org/10.1016/j.molcel.2010.09.024)

    • Search Google Scholar
    • Export Citation
  • Brodská B, Holoubek A, Otevřelová P & Kuželová K 2016 Low-dose actinomycin-D induces redistribution of wild-type and mutated nucleophosmin followed by cell death in leukemic cells. Journal of Cellular Biochemistry 117 13191329. (https://doi.org/10.1002/jcb.25420)

    • Search Google Scholar
    • Export Citation
  • Brosens JJ, Salker MS, Teklenburg G, Nautiyal J, Salter S, Lucas ES, Steel JH, Christian M, Chan YW & Boomsma CM 2014 Uterine selection of human embryos at implantation. Scientific Reports 4 3894. (https://doi.org/10.1038/srep03894)

    • Search Google Scholar
    • Export Citation
  • Bywater MJ, Poortinga G, Sanij E, Hein N, Peck A, Cullinane C, Wall M, Cluse L, Drygin D & Anderes K 2012 Inhibition of RNA polymerase I as a therapeutic strategy to promote cancer-specific activation of p53. Cancer Cell 22 5165. (https://doi.org/10.1016/j.ccr.2012.05.019)

    • Search Google Scholar
    • Export Citation
  • Cakmak H & Taylor HS 2011 Implantation failure: molecular mechanisms and clinical treatment. Human Reproduction Update 17 242253. (https://doi.org/10.1093/humupd/dmq037)

    • Search Google Scholar
    • Export Citation
  • Camus M, Lejeune B & Leroy F 1979 Induction of implantation in the rat by intraparametrial injection of lo D. Biology of Reproduction 20 11151118. (https://doi.org/10.1095/biolreprod20.5.1115)

    • Search Google Scholar
    • Export Citation
  • Cano A, Pérez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, Del Barrio MG, Portillo F & Nieto MA 2000 The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nature Cell Biology 2 7683. (https://doi.org/10.1038/35000025)

    • Search Google Scholar
    • Export Citation
  • Carotenuto P, Pecoraro A, Palma G, Russo G & Russo A 2019 Therapeutic approaches targeting nucleolus in cancer. Cells 8 1090. (https://doi.org/10.3390/cells8091090)

    • Search Google Scholar
    • Export Citation
  • Chen J & Stark LA 2018 Crosstalk between NF-kappaB and nucleoli in the regulation of cellular homeostasis. Cells 7 E157. (https://doi.org/10.3390/cells7100157)

    • Search Google Scholar
    • Export Citation
  • De Clercq K, Hennes A & Vriens J 2017 Isolation of mouse endometrial epithelial and stromal cells for in vitro decidualization. Journal of Visualized Experiments 121 55168. (https://doi.org/10.3791/55168)

    • Search Google Scholar
    • Export Citation
  • Dey SK, Lim H, Das SK, Reese J, Paria BC, Daikoku T & Wang H 2004 Molecular cues to implantation. Endocrine Reviews 25 341373. (https://doi.org/10.1210/er.2003-0020)

    • Search Google Scholar
    • Export Citation
  • Ding NZ, Qi QR, Gu XW, Zuo RJ, Liu J & Yang ZM 2018 De novo synthesis of sphingolipids is essential for decidualization in mice. Theriogenology 106 227236. (https://doi.org/10.1016/j.theriogenology.2017.09.036)

    • Search Google Scholar
    • Export Citation
  • Finn CA & Downie JM 1975 Changes in the endometrium of mice after the induction of implantation by actinomycin D. The Journal of Endocrinology 65 259264. (https://doi.org/10.1677/joe.0.0650259)

    • Search Google Scholar
    • Export Citation
  • Franco HL, Dai D, Lee KY, Rubel CA, Roop D, Boerboom D, Jeong JW, Lydon JP, Bagchi IC & Bagchi MK 2011 WNT4 is a key regulator of normal postnatal uterine development and progesterone signaling during embryo implantation and decidualization in the mouse. FASEB Journal 25 11761187. (https://doi.org/10.1096/fj.10-175349)

    • Search Google Scholar
    • Export Citation
  • Golstein P 2017 Conserved nucleolar stress at the onset of cell death. FEBS Journal 284 37913800. (https://doi.org/10.1111/febs.14095)

    • Search Google Scholar
    • Export Citation
  • Gu XW, Yan JQ, Dou HT, Liu J, Liu L, Zhao ML, Liang XH & Yang ZM 2016 Endoplasmic reticulum stress in mouse decidua during early pregnancy. Molecular and Cellular Endocrinology 434 4856. (https://doi.org/10.1016/j.mce.2016.06.012)

    • Search Google Scholar
    • Export Citation
  • Holmberg Olausson K, Nister M & Lindstrom MS 2012 p53-Dependent and -independent nucleolar stress responses. Cells 1 774798. (https://doi.org/10.3390/cells1040774)

    • Search Google Scholar
    • Export Citation
  • Hu W, Liang YX, Luo JM, Gu XW, Chen ZC, Fu T, Zhu YY, Lin S, Diao HL & Jia B 2019 Nucleolar stress regulation of endometrial receptivity in mouse models and human cell lines. Cell Death & Disease 10 831. (https://doi.org/10.1038/s41419-019-2071-6)

    • Search Google Scholar
    • Export Citation
  • James A, Wang Y, Raje H, Rosby R & Dimario P 2014 Nucleolar stress with and without p53. Nucleus 5 402426. (https://doi.org/10.4161/nucl.32235)

  • Kim TH, Yoo JY, Choi KC, Shin JH, Leach RE, Fazleabas AT, Young SL, Lessey BA, Yoon HG & Jeong JW 2019 Loss of HDAC3 results in nonreceptive endometrium and female infertility. Science Translational Medicine 11 eaaf7533. (https://doi.org/10.1126/scitranslmed.aaf7533)

    • Search Google Scholar
    • Export Citation
  • Kimura F, Takakura K, Takebayashi K, Ishikawa H, Kasahara K, Goto S & Noda Y 2001 Messenger ribonucleic acid for the mouse decidual prolactin is present and induced during in vitro decidualization of endometrial stromal cells. Gynecological Endocrinology 15 426432. (https://doi.org/10.1080/gye.15.6.426.432)

    • Search Google Scholar
    • Export Citation
  • Lei W, Feng XH, Deng WB, Ni H, Zhang ZR, Jia B, Yang XL, Wang TS, Liu JL & Su RW 2012 Progesterone and DNA damage encourage uterine cell proliferation and decidualization through up-regulating ribonucleotide reductase 2 expression during early pregnancy in mice. Journal of Biological Chemistry 287 1517415192. (https://doi.org/10.1074/jbc.M111.308023)

    • Search Google Scholar
    • Export Citation
  • Lewinska A, Bednarz D, Adamczyk-Grochala J & Wnuk M 2017 Phytochemical-induced nucleolar stress results in the inhibition of breast cancer cell proliferation. Redox Biology 12 469482. (https://doi.org/10.1016/j.redox.2017.03.014)

    • Search Google Scholar
    • Export Citation
  • Li Q, Kannan A, Das A, Demayo FJ, Hornsby PJ, Young SL, Taylor RN, Bagchi MK & Bagchi IC 2013 WNT4 acts downstream of BMP2 and functions via beta-catenin signaling pathway to regulate human endometrial stromal cell differentiation. Endocrinology 154 446457. (https://doi.org/10.1210/en.2012-1585)

    • Search Google Scholar
    • Export Citation
  • Li X, Chen H, Liu Z, Ye Z, Gou S & Wang C 2018 Overexpression of MIST1 reverses the epithelial-mesenchymal transition and reduces the tumorigenicity of pancreatic cancer cells via the Snail/E-cadherin pathway. Cancer Letters 431 96104. (https://doi.org/10.1016/j.canlet.2018.05.043)

    • Search Google Scholar
    • Export Citation
  • Liang YX, Liu L, Jin ZY, Liang XH, Fu YS, Gu XW & Yang ZM 2018 The high concentration of progesterone is harmful for endometrial receptivity and decidualization. Scientific Reports 8 712. (https://doi.org/10.1038/s41598-017-18643-w)

    • Search Google Scholar
    • Export Citation
  • Loberg MA, Bell RK, Goodwin LO, Eudy E, Miles LA, Sanmiguel JM, Young K, Bergstrom DE, Levine RL & Schneider RK 2019 Sequentially inducible mouse models reveal that Npm1 mutation causes malignant transformation of Dnmt3a-mutant clonal hematopoiesis. Leukemia 33 16351649. (https://doi.org/10.1038/s41375-018-0368-6)

    • Search Google Scholar
    • Export Citation
  • Morris EJ & Geller HM 1996 Induction of neuronal apoptosis by camptothecin, an inhibitor of DNA topoisomerase-I: evidence for cell cycle-independent toxicity. The Journal of Cell Biology 134 757770. (https://doi.org/10.1083/jcb.134.3.757)

    • Search Google Scholar
    • Export Citation
  • Nishimura K, Kumazawa T, Kuroda T, Katagiri N, Tsuchiya M, Goto N, Furumai R, Murayama A, Yanagisawa J & Kimura K 2015 Perturbation of ribosome biogenesis drives cells into senescence through 5S RNP-mediated p53 activation. Cell Reports 10 13101323. (https://doi.org/10.1016/j.celrep.2015.01.055)

    • Search Google Scholar
    • Export Citation
  • Ou HL & Schumacher B 2018 DNA damage responses and p53 in the aging process. Blood 131 488495. (https://doi.org/10.1182/blood-2017-07-746396)

    • Search Google Scholar
    • Export Citation
  • Owusu-Akyaw A, Krishnamoorthy K, Goldsmith LT & Morelli SS 2019 The role of mesenchymal-epithelial transition in endometrial function. Human Reproduction Update 25 114133. (https://doi.org/10.1093/humupd/dmy035)

    • Search Google Scholar
    • Export Citation
  • Parlato R & Liss B 2014 How Parkinson’s disease meets nucleolar stress. Biochimica et Biophysica Acta 1842 791797. (https://doi.org/10.1016/j.bbadis.2013.12.014)

    • Search Google Scholar
    • Export Citation
  • Peng M, Ding Y, Yu L, Deng Y, Lai W, Hu Y, Zhang H, Wu X, Fan H & Ding H 2015 Tegafur substitution for 5-fu in combination with actinomycin D to treat gestational trophoblastic neoplasm. PLoS One 10 e0143531. (https://doi.org/10.1371/journal.pone.0143531)

    • Search Google Scholar
    • Export Citation
  • Qi W, Shakalya K, Stejskal A, Goldman A, Beeck S, Cooke L & Mahadevan D 2008 NSC348884, a nucleophosmin inhibitor disrupts oligomer formation and induces apoptosis in human cancer cells. Oncogene 27 42104220. (https://doi.org/10.1038/onc.2008.54)

    • Search Google Scholar
    • Export Citation
  • Rutanen EM, Koistinen R, Wahlström T, Bohn H, Ranta T & Seppälä M 1985 Synthesis of placental protein 12 by human decidua. Endocrinology 116 13041309. (https://doi.org/10.1210/endo-116-4-1304)

    • Search Google Scholar
    • Export Citation
  • Schisterman EF, Mumford SL, Schliep KC, Sjaarda LA, Stanford JB, Lesher LL, Wactawski-Wende J, Lynch AM, Townsend JM & Perkins NJ 2015 Preconception low dose aspirin and time to pregnancy: findings from the effects of aspirin in gestation and reproduction randomized trial. The Journal of Clinical Endocrinology & Metabolism 100 17851791. (https://doi.org/10.1210/jc.2014-4179)

    • Search Google Scholar
    • Export Citation
  • Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Kontgen F & Abbondanzo SJ 1992 Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359 7679. (https://doi.org/10.1038/359076a0)

    • Search Google Scholar
    • Export Citation
  • Suzuki A, Kogo R, Kawahara K, Sasaki M, Nishio M, Maehama T, Sasaki T, Mimori K & Mori M 2012 A new PICTure of nucleolar stress. Cancer Science 103 632637. (https://doi.org/10.1111/j.1349-7006.2012.02219.x)

    • Search Google Scholar
    • Export Citation
  • Yang K, Wang M, Zhao Y, Sun X, Yang Y, Li X, Zhou A, Chu H, Zhou H & Xu J 2016 A redox mechanism underlying nucleolar stress sensing by nucleophosmin. Nature Communications 7 13599. (https://doi.org/10.1038/ncomms13599)

    • Search Google Scholar
    • Export Citation
  • Yang K, Yang J & Yi J 2018 Nucleolar stress: hallmarks, sensing mechanism and diseases. Cell Stress 2 125140. (https://doi.org/10.15698/cst2018.06.139)

    • Search Google Scholar
    • Export Citation
  • Zhang XH, Liang X, Liang XH, Wang TS, Qi QR, Deng WB, Sha AG & Yang ZM 2013 The mesenchymal-epithelial transition during in vitro decidualization. Reproductive Sciences 20 354360. (https://doi.org/10.1177/1933719112472738)

    • Search Google Scholar
    • Export Citation
  • Zhang Y & Lu H 2009 Signaling to p53: ribosomal proteins find their way. Cancer Cell 16 369377. (https://doi.org/10.1016/j.ccr.2009.09.024)

    • Search Google Scholar
    • Export Citation
  • Zhang Z, Ren Z, Chen S, Guo X, Liu F, Guo L & Mei N 2018 ROS generation and JNK activation contribute to 4-methoxy-TEMPO-induced cytotoxicity, autophagy, and DNA damage in HepG2 cells. Archives of Toxicology 92 717728. (https://doi.org/10.1007/s00204-017-2084-9)

    • Search Google Scholar
    • Export Citation
  • Zuo RJ, Gu XW, Qi QR, Wang TS, Zhao XY, Liu JL & Yang ZM 2015 Warburg-like glycolysis and lactate shuttle in mouse decidua during early pregnancy. Journal of Biological Chemistry 290 2128021291. (https://doi.org/10.1074/jbc.M115.656629)

    • Search Google Scholar
    • Export Citation